Superior cervical ganglion-10 protein as a molecular effectorof c-Jun N-terminal kinase 1: Implications for the therapeutic targeting of Jun N-terminal kinase in nerve regeneration

Expert Opinion on Therapeutic Targets

Volumn 12, Issue 1, 2008, Pages 31-43

  Westerlund, Nina ^a   Zdrojewska, Justyna ^a   Courtney, Michael J ^b   Coffey, Eleanor T ^a  

^a UNIVERSITY OF TURKU   (Finland)

^b UNIVERSITY OF EASTERN FINLAND   (Finland)

Author keywords

c Jun N terminal kinase; c Jun N terminal kinase 1; Cytoskeleton; Kinase; Microtubules; Neuron; Phosphorylation; Regeneration; Superior cervical ganglion 10 protein

Indexed keywords

GENE PRODUCT; GUANOSINE TRIPHOSPHATASE; MESSENGER RNA; STATHMIN; STRESS ACTIVATED PROTEIN KINASE; STRESS ACTIVATED PROTEIN KINASE 1; STRESS ACTIVATED PROTEIN KINASE INHIBITOR; SUPERIOR CERVICAL GANGLION 10 PROTEIN; UNCLASSIFIED DRUG;

BRAIN DEVELOPMENT; BRAIN REGION; CYTOSKELETON; DRUG TARGETING; ENZYME INHIBITION; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; HOMEOSTASIS; HUMAN; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MICROTUBULE; NERVE FIBER GROWTH; NERVE REGENERATION; NEUROPROTECTION; NONHUMAN; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; REVIEW; UPREGULATION;

ANIMALS; DRUG DELIVERY SYSTEMS; HUMANS; MEMBRANE PROTEINS; MICROTUBULES; MITOGEN-ACTIVATED PROTEIN KINASE 8; NERVE REGENERATION; SUPERIOR CERVICAL GANGLION;

EID: 39049167408     PISSN: 14728222     EISSN: None     Source Type: Journal    
DOI: 10.1517/14728222.12.1.31     Document Type: Review

References (84)

1. Anderson DJ, Axel R. Molecular probes for the development and plasticity of neural crest derivatives. Cell 1985;42:649-62
2. Stein R, Orit S, Anderson DJ. The induction of a neural-specific gene, SCG10 by nerve growth factor in PC12 cells is transcriptional, protein synthesis dependent, and glucocorticoid inhibitable. Dev Biol 1988;127(2):316-25
3. Mori N, Morii H. SCG10-related neuronal growth-associated proteins in neural development, plasticity, degeneration, and aging. J Neurosci Res 2002;70(3):264-73 (Review)
4. Gavet O, Ozon S, Manceau V, et al. The stathmin phosphoprotein family: intracellular localization and effects on the microtubule network. J Cell Sci 1998;111(22):3333-46
5. Ravelli RB, Gigant B, Curmi PA, et al. Insight into tubulin regulation from a complex with colchicine and a stathmin-like domain. Nature 2004;428(6979):198-202
6. Charbaute E, Curmi PA, Ozon S, et al. Stathmin family proteins display specific molecular and tubulin binding properties. J Biol Chem 2001;276(19):16146-54
7. Manna T, Grenningloh G, Miller HP, Wilson L. Stathmin family protein SCG10 differentially regulates the plus and minus end dynamics of microtubules at steady state in vitro: implications for its role in neurite outgrowth. Biochemistry 2007;46(11):3543-52
8. + channel genes binds a factor present in non-neuronal cells but not in neuronal cells. Neuron 1992;9(1):45-54
9. Schoenherr CJ, Anderson DJ. Silencing is golden: negative regulation in the control of neuronal gene transcription. Curr Opin Neurobiol 1995;5(5):566-71 (Review)
10. Watanbe H, Mizutani T, Haragucchi T, et al. SWI/SNF complex is essential for NRSF-mediated suppression of neuronal genes in human nonsmall cell lung carcinoma cell lines. Oncogene 2006;25(3):470-9
11. Walter-Yohrling J, Cao X, Callahan M, et al. Identification of genes expressed in malignant cells that promote invasion. Cancer Res 2003;63(24):8939-47
12. Paradis V, Bieche I, Dargere D, et al. Quantitative gene expression in Budd-Chiari syndrome: a molecular approach to the pathogenesis of the disease. Gut 2005;54:1776-81
13. Li S, Carmichael ST. Growth-associated gene and protein expression in the region of axonal sprouting in the aged brain after stroke. Neurobiol Dis 2006;2:362-73
14. Peng H, Derrick BE, Martinez JL Jr. Identification of upregulated SCG10 mRNA expression associated with late-phase long-term potentiation in the rat hippocampal Schaffer-CA1 pathway in vivo. J Neurosci 2003;23(16):6617-26
15. Kyriakis JM, Avruch J. Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol Rev 2001;81(2):807-69 (Review)
16. Manning AM, Davis RJ. Targeting JNK for therapeutic benefit: from junk to gold? Nat Rev Drug Discov 2003;2(7):554-65 (Review)
17. Whitmarsh AJ, Yang SH, Su MS, et al. Role of p38 and JNK mitogen-activated protein kinases in the activation of ternary complex factors. Mol Cell Biol 1997;17(5):2360-71
18. Bogoyevitch MA, Kobe B. User for JNK: the many and varied substrates of the c-Jun N-terminal kinases. Microbiol Mol Biol Rev 2006;70(4):1061-95 (Review)
19. Kuan CY, Yang DD, Samanta Roy DR, et al. The Jnk1 and Jnk2 protein kinases are required for regional specific apoptosis during early brain development. Neuron 1999;22(4):667-76
20. Sabapathy K, Jochum W, Hochedlinger K. Defective neural tube morphogenesis and altered apoptosis in the absence of both JNK1 and JNK2. Mech Dev 1999;89(1-2):115-24
21. Yang DD, Kuan CY, Whitmarsh AJ, et al. Absence of excitotoxicity-induced apoptosis in the hippocampus of mice lacking the Jnk3 gene. Nature 1997;389(6653):865-70
22. Chang L, Jones Y, Ellisman MH, et al. JNK1 is required for maintenance of neuronal microtubules and controls phosphorylation of microtubule-associated proteins. Dev Cell 2003;4(4):521-33
23. Tararuk T, Ostman N, Li W, et al. JNK1 phosphorylation of SCG10 determines microtubule dynamics and axodendritic length. J Cell Biol 2006;173(2):265-77
24. Oliva AA Jr, Atkins CM, Copenagle L, Banker GA. Activated c-Jun N-terminal kinase is required for axon formation. J Neurosci 2006;26(37):9462-70
25. Bjorkblom B, Ostman N, Hongisto V, et al. Constitutively active cytoplasmic c-Jun N-terminal kinase 1 is a dominant regulator of dendritic architecture: role of microtubule-associated protein 2 as an effector. J Neurosci 2005;25(27):6350-61
26. Hu Y, Metzler B, Xu Q. Discordant activation of stress-activated protein kinases or c-Jun NH2-terminal protein kinases in tissues of heat-stressed mice. J Biol Chem 1997;272(14):9113-19
27. Coffey ET, Hongisto V, Dickens M, et al. Dual roles for c-Jun N-terminal kinase in developmental and stress responses in cerebellar granule neurons. J Neurosci 2000;20:7602-13
28. Coffey ET, Smiciene G, Hongisto V, et al. c-Jun N-terminal protein kinase (JNK) 2/3 is specifically activated by stress, mediating c-Jun activation, in the presence of constitutive JNK1 activity in cerebellar neurons. J Neurosci 2002;22:4335-45
29. Kuan CY, Whitmarsh AJ, Yang DD, et al. A critical role of neural-specific JNK3 for ischemic apoptosis. Proc Natl Acad Sci USA 2003;100(25):15184-9
30. Barton S. Dynamic duo regulate microtubule plasticity. Nat Rev Neurosci 2006;7:421
31. Neidhart S, Antonsson B, Gillieron C, et al. c-Jun N-terminal kinase-3 (JNK3)/stress-activated protein kinase-beta (SAPKbeta) binds and phosphorylates the neuronal microtubule regulator SCG10. FEBS Lett 2001;508(2):259-64
32. Antonsson B, Lutjens R, Di Paolo G, et al. Purification, characterization, and in vitro phosphorylation of the neuron-specific membrane-associated protein SCG10. Protein Expr Purif 1997;9(3):363-71
33. Antonsson B, Kassel DB, Di Paolo G, et al. Identification of in vitro phosphorylation sites in the growth cone protein SCG10. Effect of phosphorylation site mutants on microtubule-destabilizing activity. J Biol Chem 1998;273(14):8439-46
34. Gavet O, El Messari S, Ozon S, Sobel A. Regulation and subcellular localization of the microtubule-destabilizing stathmin family phosphoproteins in cortical neurons. J Neurosci Res 2002;68:535-50
35. Niethammer P, Bastiaens P, Karsenti E. Stathmin-tubulin interaction gradients in motile and mitotic cells. Science 2004;303(5665):1862-6
36. Horwitz SB, Shen HJ, He L, et al. The microtubule-destabilizing activity of metablastin (p19) is controlled by phosphorylation. J Biol Chem 1997;272(13):8129-32
37. Stein R, Mori N, Matthews K, et al. The NGF-inducible SCG10 mRNA encodes a novel membrane-bound protein present in growth cones and abundant in developing neurons. Neuron 1988;1(6):463-76
38. Okazaki T, Wang H, Masliah E, et al. SCG10, a neuron-specific growth-associated protein in Alzheimer's disease. Neurobiol Aging 1995;16(6):883-94
39. Pellier-Monnin V, Astic L, BichetS, et al. Expression of SCG10 and stathmin proteins in the rat olfactory system during development and axonal regeneration. J Camp Neurol 2001;433(2):239-54
40. Carbani L, Carletti R, Tacconi S, et al. Differential expression of SAPK isoforms in the rat brain. An in situ hybridisation study in the adult rat brain and during post-natal development. Brain Res Mol Brain Res 1998;60(1):57-68
41. Ozon S, Guichet A, Gavet O, Roth S, et al. Drosophila stathmin: a microtubule-destabilizing factor involved in nervous system formation. Mol Biol Cell 2002;13(2):698-10
42. Baldassare G, Belletti B, Nicoloso MS, et al. p27(Kip1)-stathmin interaction influences sarcoma cell migration and invasion. Cancer Cell 2005;7(1):51-63
43. Xia Y, Karin M. The control of cell motility and epithelial morphogenesis by Jun kinases. Trends Cell Biol 2004;14(2):94-101 (Review)
44. Thuret S, Moon LD, Gage FH. Therapeutic interventions after spinal cord injury. Nat Rev Neurosci 2006;7(8):628-43 (Review)
45. Raisman G, Li Y. Repair of neural pathways by olfactory ensheathing cells. Nat Rev Neurosci 2007;8(4):312-19 (Review)
46. Camoletto P, Colesanti A, Own S, et al. Expression of stathmin and SCG10 proteins in the olfactory neurogenesis during development and after lesion in the adulthood. Brain Res Bull 2001;54(1):19-28
47. Carmichael ST, Archibeque I, Luke L, et al. Growth-associated gene expression after stroke: evidence for a growth-promoting region in peri-infarct cortex. Exp Neurol 2005;193(2):291-311
48. Mason MR, Lieberman AR, Grenningloh G, Anderson PN. Transcriptional upregulation of SCG10 and CAP-23 is correlated with regeneration of the axons of peripheral and central neurons in vivo. Mol Cell Neurosci 2002;20(4):595-615
49. Mason MR, Lieberman AR, Anderson PN. Corticospinal neurons up-regulate a range of growth-associated genes following intracortical, but not spinal, axotomy. Eur J Neurosci 2003;18(4):789-802
50. Snider WD, Thanedar S. Target dependence of hypoglossal motor neurons during development in maturity. J Comp Neurol 1989;279(3):489-98
51. Iwata T, Namikawa K, Honma M, et al. Increased expression of mRNAs for microtubule disassembly molecules during nerve regeneration. Brain Res Mol Brain Res 2002;102(1-2):105-9
52. Voria I, Hauser J, Axis A, et al. Improved sciatic nerve regeneration by local thyroid hormone treatment in adult rat is accompanied by increased expression of SCG10. Exp Neurol 2006;197:258-67
53. Suh LH, Oster SF, Soehrman SS, et al. L1/Laminin modulation of growth cone response to EphB triggers growth pauses and regulates the microtubule destabilizing protein SCG10. J Neurosci 2004;24(8):1976-86
54. Liedtke W, Leman EE, Fyffe RE, et al. Stathmin-dedicient mice develop an age-dependent axonopathy of the central and peripheral nervous systems. Am J Pathol 2002;160(2):469-80
55. Brecht S, Kirchof R, Chromik A, et al. Specific pathophysiological functions of JNK isoforms in the brain. Eur J Neurosci 2005;21(2):363-77
56. Yoshida K, Behrens A, Le-Niculescu H, et al. Amino-terminal phosphorylation of c-Jun regulates apoptosis in the retinal ganglion cells by optic nerve transection. Invest Ophthalmol Vis Sci 2002;43(5):1631-5
57. Lindvall C, Kanje M. Retrograde axonal transport of JNK signaling molecules influence injury induced nuclear changes in p-c-Jun and ATF3 in adult rat sensory neurons. Mol Cell Neurosci 2005;29(2):269-82
58. Waetzig V, Zhao Y, Herdegen T. The bright side of JNKs-multitalented mediators in neuronal sprouting, brain development and nerve fiber regeneration. Prog Neurobiol 2006;80(2):84-97 (Review)
59. Kenney AM, Kocsis JD. Peripheral axotomy induces long-term c-Jun amino-terminal kinase-1 activation and activator protein-1 binding activity by c-Jun and junD in adult rat dorsal root ganglia in vivo. J Neurosci 1998;18(4):1318-28
60. Cavalli V, Kujala P, Kluperman J, Goldstein LS. Sunday Driver links axonal transport to damage signaling. J Cell Biol 2005;168(5):775-87
61. Whitmarsh AJ, Kuan CY, Kennedy NJ, et al. Requirement of the JIP1 scaffold protein for stress-induced JNK activation. Genes Dev 2001;15(18):2421-32
62. Verhey KJ, Meyer D, Deehan R, et al. Cargo of kinesin identified as JIP scaffolding proteins and associated signaling molecules. J Cell Biol 2001;152(5):959-70
63. Herdegen T, Skene P, Bahr M. The c-Jun transcription factor - bipotential mediator of neuronal death, survival and regeneration. Trends Neurosci 1997;20(5):227-31
64. Lindvall C, Kanje M. The role of p-c-Jun in survival and outgrowth of developing sensory neurons. Neuroreport 2005;16(15):1655-9
65. Raivich G, Behrens A. Role of the AP-1 transcription factor c-Jun in developing, adult and injured brain. Prog Neurobiol 2006;78(6):347-63 (Review)
66. Cameron HA, McKay RD. Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J Comp Neurol 2001;435(4):406-17
67. Grafe MR. Developmental factors affecting regeneration in the central nervous system: early but not late formed mitral cells reinnervate olfactory cortex after neonatal tract section. J Neurosci 1983;3(3):617-30
68. Riederer BM, Pellier V, Antonsson B, et al. Regulation of microtubule dynamics by the neuronal growth-associated protein SCG10. Proc Natl Acad Sci USA 1997;94(2):741-5
69. Morii H, Shirashi-Yamaguchi, Mori N. SCG10, a microtubule destabilizing factor, stimulates the neurite outgrowth by modulating microtubule dynamics in rat hippocampal primary cultured neurons. J Neurobiol 2006;66(10):1101-14
70. Curmi PA, Gavet O, Charbaut E, et al. Stathmin and its phosphoprotein family: general properties, biochemical and functional interaction with tubulin. Cell Struct Funct 1999;5:345-57
71. Gigant B, Curmi PA, Martin-Barbey C, et el. The 4 A X-ray structure of a tubulin:stathmin-like domain complex. Cell 2000;02:809-16
72. Brannstrom K, Segerman B, Gullberg M. Molecular dissection of GTP exchange and hydrolysis within the ternary complex of tubulin heterodimers and Op18/stathmin family members. J Biol Chem 2003;278(19):16651-7
73. Wang C, Cormier A, Gigant B, Knossow M. Insight into the GTPase Activity of Tubulin from Complexes with Stathmin-Like Domains. Biochemistry 2007 published online August 21st 2007, DOI: 10.1021/bi701147f
74. Kikkawa M, Metlagel Z. A molecular "zipper" for microtubules. Cell 2006;127(7):1302-4
75. Bennett BL, Satoh Y, Lewis AJ. JNK: a new therapeutic target for diabetes. Curr Opin Pharmacol 2003;3(4):420-25 (Review)
76. Borsello T, Clarke PG, Hirt L, et al. A peptide inhibitor of c-Jun N-terminal kinase protects against excitotoxicity and cerebral ischemia. Nat Med 2003;9(9):1180-6
77. Kaneto H, Nakatani Y, Miyatsuka T, et al. Possible novel therapy for diabetes with cell-permeable JNK-inhibitory peptide. Nat Med 2004;10:1128-32
78. Ma FY, Flanc RS, Teach GH, et al. A pathogenic role for c-Jun amino-terminal kinase signaling in renal fibrosis and tubular cell apoptosis. J Am Soc Nephrol 2007;18(2):472-84
79. Erturk A, Hellal F, Enes J, Bradke F. Disorganized microtubules underlie the formation of retraction bulbs and the failure of axonal regeneration. J Neurosci 2007;27(34):9169-80
80. Gordon-Weeks PR, Fischer I. MAP1B expression and microtubule stability in growing and regenerating axons. Microsc Res Tech 2000;48:63-74 (Review)
81. Gonzalez-Billault C, Jimenez-Mateos EM, Caceres A, et al. Microtubule-associated protein 1B function during normal development, regeneration, and pathological conditions in the nervous system. J Neurobiol 2004;58:48-59 (Review)
82. Book AA, Fischer I, Yu XJ, et al. Altered expression of microtubule-associated proteins in cat trochlear motoneurons after peripheral and central lesions of the trochlear nerve. Exp Neurol 1996;138(2):214-26
83. Bush MS, Tonge DA, Woolf C, Gordon-Weeks PR. Expression of a developmentally regulated, phosphorylated isoform of microtubule-associated protein 1B in regenerating axons of the sciatic nerve. Neuroscience 1996;73:553-63
84. Sandblad L, Busch KE, Tittmann P, et al. The Schizosaccharomyces pombe EB1 homolog Mal3p binds and stabilizes the microtubule lattice seam. Cell 2006;127(7):1415-24